Appropriately for a set of institutions with no single leader, the EU sent three of its presidents to collect the award at a ceremony in Oslo's City Hall attended by 20 EU heads of state and government.
Archbishop Desmond Tutu, who won the prize in 1984 for his campaign against South African apartheid, said it was wrong to recognise the EU as it was an organisation based on "military force", and others have criticised the decision because the bloc is mired in economic and financial crisis.
But the Norwegian Nobel committee that bestows the award focused on what the EU had achieved over the past six decades to bring peace and security to once-warring nations, and to stitch back together the torn fabric of the "old continent".
Herman Van Rompuy, the president of the European Council that represents EU leaders, invoked his own family history to highlight how raw the memories of World War Two remain.
"As a child born in Belgium just after the war, I heard the stories first hand," he said in his acceptance speech. "In 1940, my father, then 17, had to dig his own grave. He got away; otherwise I would not be here today.
"So what a bold bet it was for Europe's founders to say, yes, we can break this endless cycle of violence, we can stop the logic of vengeance, we can build a brighter future."
During the ceremony, German Chancellor Angela Merkel and French President Francois Hollande sat next to each other in the front row, occasionally smiling and chatting, as if to underline how enmities of old can be transformed into alliances.
But British Prime Minister David Cameron, whose relationship with the EU is increasingly troubled, did not attend the ceremony. Instead he went to a lunch with journalists in the British parliament and joked about not being in Norway.
"Thank you for giving me an excuse not to be there for the great jamboree in Oslo," he told the reporters, while adding that he did not want Britain to leave the European Union.
CONTINENT IN CRISIS
Many people still find it difficult to understand why the EU and its 27 member states should receive the award.
Europe is suffering feeble economic growth or recession, soaring unemployment and a number of countries that share the single currency are unable to pay their debts. It has been called the worst economic crisis since World War Two.
The financial pain has provoked social unrest in a number of member states, notably near-bankrupt Greece, and in many countries the European Union has become a byword for disorder and mismanagement, not democracy and human rights.
However, in its citation, the Nobel committee focused on the EU's role in reconciling old hatreds, with the emphasis on how Germany and France had overcome their past to stand together.
From just six countries which agreed to pool their coal and steel production in the 1950s, the EU now stretches from Portugal to Romania, Finland to Malta and sets rules and regulations that have a bearing on more than 500 million people.
"The stabilizing part played by the EU has helped to transform most of Europe from a continent of war to a continent of peace," the Nobel committee said on October 12 when it announced the EU had won, an unexpected decision.
"The division between East and West has to a large extent been brought to an end; democracy has been strengthened; many ethnically based national conflicts have been settled."
European Commission President Barroso, a former prime minister of Portugal who was part of the struggle to turn his country into a democracy in 1974, echoed those sentiments.
"It's a recognition of what has been achieved over the 60 years and at the same time, it's also an encouragement for the future," he told Reuters. "I think the message they give to us is that what you have built is something very precious, something that we should treasure, that we should keep."
The EU drew heavy criticism along with other Western powers in the 1990s for failing to intervene rapidly in a series of wars on its doorstep as Yugoslavia collapsed. However, it has since played a leading role in peacekeeping there and one former Yugoslav republic, Slovenia, is now an EU member while another, Croatia, is scheduled to join next year.
0.2 EURO CENTS EACH
The Nobel prize money of 930,000 euros ($1.25 million) will be given to projects that help children struggling in war zones, with the recipients to be announced next week. The EU has said it will match the prize money, so that a total of 2 million euros will be given to the selected aid projects.
That decision went some way to silence critics on Twitter and other social media sites who initially joked that if the award was for all Europeans then they should all share the prize money - which would equal about 0.2 euro cents each.
Commentators on social media haven't been the only critics of the award going to the EU.
Tutu was joined in his opposition by two other recipients, and on Sunday around 1,000 members of left-wing and human-rights groups marched through Oslo in protest, saying the EU was not a rightful beneficiary under the terms Alfred Nobel laid down in his 1895 will.
"Alfred Nobel said that the prize should be given to those who worked for disarmament," said Elsa-Britt Enger, 70, a representative of Grandmothers for Peace. "The EU doesn't do that. It is one of the biggest weapons producers in the world."
The biggest challenge for the EU, beyond maintaining the peace and security it has helped foster, is to keep itself relevant and meaningful in a rapidly changing world.
Next year the union will expand to 28 members as Croatia joins and there are others in the Western Balkans which are keen to become members. But Britain, which joined in 1973, is increasingly doubtful about its own role in Europe, and the risk remains that a euro zone country could leave the currency bloc.
Speaking before he accepted the prize, Van Rompuy said it was not just about recognising the past but about giving European leaders a reason to pursue ever-closer union.
"It is not only rewarding past achievements, it is also an encouragement to go further and to work further on deepening the European Union," Van Rompuy said. "The answer is more Europe and more integration."
(Additional reporting by Balazs Koranyi and Vegard Botterli; Editing by David Stamp)